THE SPOTTED SANDGROUSE, PTEROCLES SENEGALLUS (LINNAEUS, 1771) AS A NEW HOST FOR THE SPIRURID NEMATODE HARTERTIA GALLINARUM (THEILER, 1919) IN IRAQ
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1 Bull. Iraq nat. Hist. Mus. (2017) 14 (3): Mohammad K. Mohammad and Azhar A. Al-Moussawi THE SPOTTED SANDGROUSE, PTEROCLES SENEGALLUS (LINNAEUS, 1771) AS A NEW HOST FOR THE SPIRURID NEMATODE HARTERTIA GALLINARUM (THEILER, 1919) IN IRAQ Mohammad K. Mohammad and Azhar A. Al-Moussawi* Iraq Natural History Research Centre and Museum, University of Baghdad, Baghdad, Iraq *Corresponding Author: azhar.nhm@gmail.com Received Date: 16.March.2017 Accepted Date: : 24.April.2017 ABSTRACT In this work, the spirurid nematode Hartertia gallinarum was reported in the intestine of the spotted sandgrouse, Pterocles senegallus, collected in three different locations: Ga'ara Depression, Iraqi Western Desert, Zurbatiyah and Al-Attariyah, Middle of Iraq. Description and measurements of the nematode were given. The role of termites in the infection of P. senegallus with H. gallinarum was discussed. Occurrence of H. gallinarum in P. senegallus represents a new host record. Key words: Hartertia, Iraq, Pterocles, Spotted sandgrouse, Termite. INTRODUCTION The spotted Sandgrouse Pterocles senegallus is a common and widely distributed bird (Bolster, 1922) found in North Africa and Middle East, and it is a native bird in Iraq (BirdLife International, 2016). It inhabits mainly sand deserts and semi deserts with scattered plants and breeds nesting on ground in suitable areas of the middle and southern Iraq (Salim et al., 2006). This species is considered as one of the most popular game birds in its distribution range in Iraq. The nematode Hartertia gallinarum (Theiler, 1919) is distributed in South and West Africa and Asia. It causes host diarrhea, weight loss, weakness and decreased egg production and losses of the bird host (Kaufmann, 1996). In Iraq, Al-Hubaity (1976) found H. gallinarum in fowl Gallus gallus domesticus in Mousl, north of Iraq. Then it has been isolated from the caecum of Rock partridge, Alectoris graeca and from the gizzard, proventriculus, intestine and liver of Seesee partridge, Ammoperdix griseogularis in the Gara-area, Rutba, western desert district respectively (Mohammad, 1996; Mahmoud et al., 2000). Later, Khoshnaw and Abdullah (2013) recorded it in the caecum of chukar partridge Alectoris chukar in Shaqlawa district, Kurdistan region, North of Iraq. The present paper deals with recording the nematode H. gallinarum from the intestine of P. senegallus for the first time in Iraq. 205
2 The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host MATERIALS AND METHODS A total of 16 spotted Sandgrouse, Pterocles senegallus (10 males and 6 females) were collected in three different locations; Ga'ara Depression, Iraqi Western Desert (7 males and 4 females), Zurbatiyah (1 male and 1 female) and Al-Attariyah (2 males and 1 female), Middle of Iraq (Map 1). Collection of birds was done during January-December 2016 in Zurbatiyah and Al-Attariyah while those of Ga'ara were previously collected during the years Gastrointestinal tracts of the collected animals were excised, opened longitudinally and nematodes were removed, washed with physiological saline, fixed in 70% alcohol, cleared in lactopheno and identified morphologically based on the available keys and descriptions (Cram, 1927; Yamaguti, 1961). All measurements are in millimeters given as means followed by ranges in parentheses. Photomicrographs were taken with a digital camera Infinity lite- K100 attached to compound microscope Micros MCX100. Map (1): Showing the collection sites of host birds from different regions of Iraq. RESULTS AND DISCUSSION Order Spirurata Family Spiruridae Genus Hartertia Seurat, Hartertia gallinarum (Theiler, 1919) Cram, Synonym: Filaria gallinarum Theiler, (Cram, 1927). Only specimens of the spotted sandgrouse, P. senegallus from Ga'ara Depression were infected with 29 specimens of H. gallinarum, 3 males and 26 females with an infection rate of 100% while the rest of the host samples yielded no parasites. The total infection rate was 206
3 Mohammad K. Mohammad and Azhar A. Al-Moussawi 68.75% with intensity of According to Encyclopedia of Life (2017), GBIF (2017) and Fauna Europaea (2017), this nematode belongs to the order Spirurata and the family Hartertiidae. It has one synonym which is Filaria gallinarum Theiler, The worm is filiform attenuating at each extremity. Cuticle thick is finely striated transversely. Head small with a slight constriction. Two lips are trilobed and each lip toothed, with a lateral papilla and lined by a thick cuticle. Two cervical papillae just behind the lips. The pyriform vestibule is short. Esophagus is divided into two parts; the anterior one is short and muscular. The posterior is longer and glandular. Male (Pl. 1, 2 and 3): Three males were isolated, each with symmetrical caudal alae. Six pedunculated papillae, four pairs are preanal. Measurements of three specimens were: Body is ( ) long x 0.79 ( ) maximum wide. Cephalic papillae is situated at a distance of ( ) far from the anterior extremity of the body. Pyriform vestibule is ( ) long x ( ) wide. Oesophagus reaches long in one specimen in which body length was Oesophagus length as a proportion of body length is Nerve ring ( ) long x ( ) wide, at a distance of ( ) far from anterior extremity. Six pairs of pedunculated papillae, of which four precloacal and two postcloacal and group of very small sessile papillae present at tip of the tail. Spicules unequal, right spicule is ( ), the left spicule is (measurements for two specimens only) ( ) long. Tail length is ( ). Tail length as a proportion of body length is ( ). Female (Pl. 4, 5): Twenty-six females were isolated. They are larger than males. Body is ( ) long x ( ) maximum wide. Head is ( ) long x ( ) wide. Tooth at a distance of ( ) from anterior extremity of the body. Cervical papillae are situated at a distance of ( ) from anterior extremity. The vestibule is ( ) long x ( ) wide. Excretory pore is situated at ( ) from anterior extremity. Oesophagus is ( ). Oesophagus as a proportion of body length is ( ). Nerve ring is ( ) long x ( ) wide, at distance of ( ) from anterior extremity. Vulva distance from anterior extremity is ( ). The embryonated eggs have thick double shell. Tail is conical, rounded at its end and ( ) long. The morphology of H. gallinarum in the present study did not show differences from H. gallinarum found in Cram (1927) but there are some differences in measurements between the present specimens and those of Cram (1927) as well as with those of the other local studies by (Al-Hubaity, 1976; Mohammad, 1996; Mahmoud et al., 2000; Khoshnaw and Abdullah, 2013) which had been isolated from different bird species belonging to another order. Presence of the same species of parasites in different host species may induce some morphological variations (Hildebrand et al., 2015) and / or physiological variations (Mehlhorn, 2016). It is worth to mention that Mohammad (1996) had reported this nematode from Alectoris graeca. This host was proved later to be A. chukar according to Salim et al. (2006). So, the hosts examined by Mohammad (1996) and Khoshnaw and Abdullah (2013) were actually the same bird species (A. chukar). Occurrence of H. gallinarum in P. senegallus of the present investigation represents a new host record in Iraq and to the best of our knowledge it is the first time that this parasite has ever been recorded from members of the family Pteroclididae (Order, Pterocliformes). Regarding transmitting of H. gallinarum to its present host which depends only on small seeds (Bolster, 1922), we have now only indirect evidence that the 207
4 The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host spotted sandgrouse P. senegallus eats ants and termites during its breeding season (Campbell and Lack, 1985) probably because protein is required for egg laying, incubation activities and chick growing. It is necessary to reveal this subject through crop analyses of a good number of male and female individuals of this bird collected from different parts of its distribution range in Iraq. It seems necessary also to investigate about another species of parasites infecting this game bird from the human health viewpoint since large numbers of the bird are eaten every year by humans. The nematode H. gallinarum infects chicken and other birds (Baker, 1973). To complete its life cycle, it requires termites (Kaufmann, 1996). Babaeian and Zangiband (2014) found that this nematode needs the termite Anacanthotermes ubachi for its development. A. ubachi (found in Ga'ara Depression) and two other Anacanthotermes species: A. vagans and A. sawensis were previously recorded in Iraq by Al-Alawy (1987). Plate (1): Anterior end of male of Hartertia gallinarum. 208
5 Mohammad K. Mohammad and Azhar A. Al-Moussawi Plate (2): Head of male of H. gallinarum (lateral view) Plate (3): Tail of male of H. gallinarum 209
6 The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host Plate (4): Anterior end of female of H. gallinarum Plate (5): Posterior end of female of H. gallinarum 210
7 Mohammad K. Mohammad and Azhar A. Al-Moussawi LITERATURE CITED Al-Alawy, S.A Taxonomical and ecological studies on termites Insecta, Isoptera in Iraq. Ph. D. Thesis, Department of Plant Protection, College of Agriculture, University of Baghdad, 223pp. Al-Hubaity, I.A Studies on the parasites of fowl Gallus gallus domesticus in Mousl district, Iraq. Mesopotamia Journal of Agriculture, 14(1): Babaeian, A. and Zangiband, P A study of gastrointestinal helminth parasites of wild red-legged partridges (Alectoris rufa) from Kurdistan province, Iran. 8 th International congress of Clinical Microbiology, Tabriz-Iran 30 Sep - 2 Oct Baker, D.G Flynn s Parasites of Laboratory Animals. Blackwell Publishing Publications, Oxford, 813pp. Bird Life International, Pterocles senegallus. The IUCN Red List of Threatened Species 2016:e.T A (Accessed 12 March 2017). Bolster, R.C The occurrence, habits and breeding of the spotted sandgrouse (Pteroclurus senegallus) in the Bahawalpur State, Punjab. The journal of the Bombay Natural History Society, 28: Campbell, B. and Lack, E. (Eds.) A Dictionary of Birds. Buteo Books. Published for the British Ornithologists's Union. 1 st ed., T. and A. D. Poyser, Ltd., Carlton, UK,700pp. ISBN Cram, E.B Bird parasites of the nematode suborders Strongylata, Ascaridata and Spirurata. Bulletin of the United States National Museum, 140: 464pp. EOL Encyclopedia of Life on-line database, http// (Accessed 18 April 2017). Fauna Europaea Accessed via on DOI: /ymk1bx. GBIF Accessed via on DOI: /39omei. Hildebrand, J., Adamczyk, M., Laskowski, Z. and Zaleśny, G Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Lühe, 1909 (Digenea, Echinostomatinae): Morphological variation vs. molecular stability. Parasite and Vectors, 8: 481. Kaufmann, J Parasitic Infections of Domestic Animals: A Diagnostic Manual. Springer Basel, xvi + 423pp. 211
8 The spotted sandgrouse, Pterocles senegallus (Linnaeus, 1771) as a new host Khoshnaw, Z.O.I. and Abdullah, S.M.A Study on the parasites of chukar partridge Alectoris chukar from Shaqlawa district, Kurdistan region, Iraq. Tikrit Journal of Pure Science, 18(3): Mahmoud, S.S., Mohammad, M.K. and Ali, S.Y Intensity and histopathological effects of the nematode Hartertia gallinarum (Theiler, 1919) on seesee partridge, Ammoperdix griseogularis (Brandt, 1843) collected from Qaara area, west of Iraq. Bulletin of the Iraq Natural History Museum, 9(2): Mehlhorn, H Animal Parasites: Diagnosis, Treatment, Prevention. Springer International Publishing, XVII, 719pp. Mohammad, M.K Intestinal helminth parasites of the rock partridge Alectoris graeca in G'ara area, west of Iraq. Bulletin of the Iraq Natural History Museum, 8(4): Salim, M.A., Porter, R.F., Christensen, S., Schiermacker-Hansen, P. and Al-Jbour, S Field Guide to the Birds of Iraq. Nature Iraq and Bird Life International, Amman, 284 pp. (In Arabic). Yamaguti, S Systema Helminthum. Vol. 3. The Nematodes of Vertebrates, Part I + II. Interscience Publisher, Inc., New York, 1261pp. 212
9 Mohammad K. Mohammad and Azhar A. Al-Moussawi Bull. Iraq nat. Hist. Mus. (2017) 14 (3): القطا المرقط (1771 (Linnaeus, Pterocles senegallus كمض يف جديد للدودة الخيطية 1919) (Theiler, Hartertia gallinarum في وسط العراق محمد كاظم محمد و ازهار احمد سعد هللا مركز بحوث و متحف التأريخ الطبيعي جامعة بغداد بغداد العراق تأريخ االستالم: 2017/03/16 تأريخ القبول: 2017/04/24 الخالصة هذا البحث معني بظهور الدودة الخيطية Hartertia gallinarum من أمعاء القطا المرقط Pterocles senegallus الذي جمع من منخفض القعرة في غرب العراق ومن زرباطية والعطارية في وسط العراق. أعطي وصف وقياسات تلك الدودة الخيطية كما ألقي الضوء على دور النمل األبيض Anacanthotermes ubachi في إصابة القطا المرقط بتلك الدودة الخيطية. بموجب الدراسة الحالية يعتبر القطا المرقط مضي فا جديدا لهذه الدودة الخيطية في العراق. 213
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